DNA Geminivirus Infection Induces an Imprinted E3 Ligase Gene to Epigenetically Activate Viral Gene Transcription

Abstract

Flowering plants and mammals contain imprinted genes that are primarily expressed in the endosperm and placenta in a parent-of-origin manner. In this study, we show that early activation of the geminivirus genes <i>C2</i> and <i>C3</i> in Arabidopsis (<i>Arabidopsis thaliana</i>) plants, encoding a viral suppressor of RNA interference and a replication enhancer protein, respectively, is correlated with the transient vegetative expression of <i>VARIANT IN METHYLATION5</i> (<i>VIM5</i>), an endosperm imprinted gene that is conserved in diverse plant species. VIM5 is a ubiquitin E3 ligase that directly targets the DNA methyltransferases MET1 and CMT3 for degradation by the ubiquitin-26S proteasome proteolytic pathway. Infection with <i>Beet severe curly top virus</i> induced <i>VIM5</i> expression in rosette leaf tissues, possibly via the expression of the viral replication initiator protein, leading to the early activation of <i>C2</i> and <i>C3</i> coupled with reduced symmetric methylation in the <i>C2-3</i> promoter and the onset of disease symptoms. These findings demonstrate how this small DNA virus recruits a host imprinted gene for the epigenetic activation of viral gene transcription. Our findings reveal a distinct strategy used by plant pathogens to exploit the host machinery in order to inhibit methylation-mediated defense responses when establishing infection.